Mitochondrial efficiency is increased in axenically cultured Caenorhabditis elegans

Experimental Gerontology

Volumn 56, Issue , 2014, Pages 26-36

  Castelein, Natascha ^a   Muschol, Michael ^b   Dhondt, Ineke ^a   Cai, Huaihan ^a   De Vos, Winnok H ^a,c   Dencher, Norbert A ^b   Braeckman, Bart P ^a  

^a GHENT UNIVERSITY   (Belgium)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Axenic; Bioenergetics; Caenorhabditis elegans; Dietary restriction; Mitochondria; ROS

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; MULTIENZYME COMPLEX;

AGING; ARTICLE; AXENIC CULTURE; AXENIC DIETARY RESTRICTION; BIOENERGY; CAENORHABDITIS ELEGANS; CELL FUNCTION; CONTROLLED STUDY; COUPLING FACTOR; DIET RESTRICTION; IN VIVO STUDY; LIFESPAN; MITOCHONDRIAL DENSITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RESPIRATORY CHAIN; AGE; ANIMAL; CALORIC RESTRICTION; ENERGY METABOLISM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OXIDATIVE STRESS;

ANIMALIA; CAENORHABDITIS ELEGANS;

AGE FACTORS; AGING; ANIMALS; AXENIC CULTURE; CAENORHABDITIS ELEGANS; CALORIC RESTRICTION; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ENERGY METABOLISM; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84901831094     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2014.02.009     Document Type: Article

References (67)

1. Acin-Perez R., Fernandez-Silva P., Peleato M.L., Perez-Martos A., Enriquez J.A. Respiratory active mitochondrial supercomplexes. Mol. Cell 2008, 32:529-539.
2. Back P., Braeckman B.P., Matthijssens F. ROS in aging Caenorhabditis elegans: damage or signaling?. Oxidative Med. Cell. Longev. 2012, 608478.
3. Back P., De Vos W.H., Depuydt G.G., Matthijssens F., Vanfleteren J.R., Braeckman B.P. Exploring real-time in vivo redox biology of developing and aging Caenorhabditis elegans. Free Radic. Biol. Med. 2012, 52:850-859.
4. Bevilacqua L., Ramsey J.J., Hagopian K., Weindruch R., Harper M.E. Long-term caloric restriction increases UCP3 content but decreases proton leak and reactive oxygen species production in rat skeletal muscle mitochondria. Am. J. Physiol. Endocrinol. Metab. 2005, 289:E429-E438.
5. Bishop N.A., Guarente L. Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 2007, 447:545-549.
6. Blachly-Dyson E., Forte M. VDAC channels. IUBMB Life 2001, 52:113-118.
7. Brand M.D. Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp. Gerontol. 2000, 35:811-820.
8. Brys K., Castelein N., Matthijssens F., Vanfleteren J.R., Braeckman B.P. Disruption of insulin signalling preserves bioenergetic competence of mitochondria in ageing Caenorhabditis elegans. BMC Biol. 2010, 8:91.
9. Castelein N., Hoogewijs D., De Vreese A., Braeckman B.P., Vanfleteren J.R. Dietary restriction by growth in axenic medium induces discrete changes in the transcriptional output of genes involved in energy metabolism in Caenorhabditis elegans. Biotechnol. J. 2008, 3:803-812.
10. Chance B., Williams G.R. A method for the localization of sites for oxidative phosphorylation. Nature 1955, 176:250-254.
11. Civitarese A.E., Carling S., Heilbronn L.K., Hulver M.H., Ukropcova B., Deutsch W.A., Smith S.R., Ravussin E. Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med. 2007, 4:e76.
12. Dani D., Shimokawa I., Komatsu T., Higami Y., Warnken U., Schokraie E., Schnolzer M., Krause F., Sugawa M.D., Dencher N.A. Modulation of oxidative phosphorylation machinery signifies a prime mode of anti-ageing mechanism of calorie restriction in male rat liver mitochondria. Biogerontology 2010, 11:321-334.
13. Davies K.M., Anselmi C., Wittig I., Faraldo-Gomez J.D., Kuhlbrandt W. Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:13602-13607.
14. Dillin A., Hsu A.L., Arantes-Oliveira N., Lehrer-Graiwer J., Hsin H., Fraser A.G., Kamath R.S., Ahringer J., Kenyon C. Rates of behavior and aging specified by mitochondrial function during development. Science 2002, 298:2398-2401.
15. Frenzel M., Rommelspacher H., Sugawa M.D., Dencher N.A. Ageing alters the supramolecular architecture of OxPhos complexes in rat brain cortex. Exp. Gerontol. 2010, 45:563-572.
16. Gnaiger E. Mitochondrial pathways and respiratory control. An introduction to OXPHOS analysis. Mitochondrial Physiol. Netw. 2012, 17(18).
17. Greer E.L., Brunet A. Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 2009, 8:113-127.
18. Groebe K., Krause F., Kunstmann B., Unterluggauer H., Reifschneider N.H., Scheckhuber C.Q., Sastri C., Stegmann W., Wozny W., Schwall G.P., Poznanovic S., Dencher N.A., Jansen-Durr P., Osiewacz H.D., Schrattenholz A. Differential proteomic profiling of mitochondria from Podospora anserina, rat and human reveals distinct patterns of age-related oxidative changes. Exp. Gerontol. 2007, 42:887-898.
19. 2-scavenging peroxidases. J. Biol. Chem. 2009, 284:31532-31540.
20. Hakimi P., Yang J., Casadesus G., Massillon D., Tolentino-Silva F., Nye C.K., Cabrera M.E., Hagen D.R., Utter C.B., Baghdy Y., Johnson D.H., Wilson D.L., Kirwan J.P., Kalhan S.C., Hanson R.W. Overexpression of the cytosolic form of phosphoenolpyruvate carboxykinase (GTP) in skeletal muscle repatterns energy metabolism in the mouse. J. Biol. Chem. 2007, 282:32844-32855.
21. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 1956, 11:298-300.
22. Harman D. The biologic clock: the mitochondria?. J. Am. Geriatr. Soc. 1972, 20:145-147.
23. Hempenstall S., Page M.M., Wallen K.R., Selman C. Dietary restriction increases skeletal muscle mitochondrial respiration but not mitochondrial content in C57BL/6 mice. Mech. Ageing Dev. 2012, 133:37-45.
24. Houthoofd K., Braeckman B.P., Lenaerts I., Brys K., De Vreese A., Van Eygen S., Vanfleteren J.R. Axenic growth up-regulates mass-specific metabolic rate, stress resistance, and extends life span in Caenorhabditis elegans. Exp. Gerontol. 2002, 37:1371-1378.
25. Houthoofd K., Braeckman B.P., Lenaerts I., Brys K., De Vreese A., Van Eygen S., Vanfleteren J.R. No reduction of metabolic rate in food restricted Caenorhabditis elegans. Exp. Gerontol. 2002, 37:1359-1369.
26. Houthoofd K., Braeckman B.P., Johnson T.E., Vanfleteren J.R. Life extension via dietary restriction is independent of the Ins/IGF-1 signalling pathway in Caenorhabditis elegans. Exp. Gerontol. 2003, 38:947-954.
27. Hsin H., Kenyon C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature 1999, 399:362-366.
28. Krause F., Seelert H. Detection and analysis of protein-protein interactions of organellar and prokaryotic proteomes by blue native and colorless native gel electrophoresis. Current Protocols in Protein Science/editorial Board 2008, (Chapter 14:Unit 14 11). J.E. Coligan (Ed.).
29. Lal S.B., Ramsey J.J., Monemdjou S., Weindruch R., Harper M.E. Effects of caloric restriction on skeletal muscle mitochondrial proton leak in aging rats. J. Gerontol. A Biol. Sci. Med. Sci. 2001, 56:B116-B122.
30. Lambert A.J., Merry B.J. Effect of caloric restriction on mitochondrial reactive oxygen species production and bioenergetics: reversal by insulin. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286:R71-R79.
31. Lanza I.R., Zabielski P., Klaus K.A., Morse D.M., Heppelmann C.J., Bergen H.R., Dasari S., Walrand S., Short K.R., Johnson M.L., Robinson M.M., Schimke J.M., Jakaitis D.R., Asmann Y.W., Sun Z., Nair K.S. Chronic caloric restriction preserves mitochondrial function in senescence without increasing mitochondrial biogenesis. Cell Metab. 2012, 16:777-788.
32. Le Pécheur M., Morrow G., Kim H.-J., Schäfer E., Dencher N., Tanguay R.M. Characterization of OXPHOS complexes in long-lived flies overexpressing Hsp22. Mitochondria in Ageing and Age-related Disease, MiMage Final Meeting (and LINK-AGE Topic Research) Group Meeting Abstract 2009, 16.
33. Lemire B.D., Behrendt M., DeCorby A., Gaskova D. C. elegans longevity pathways converge to decrease mitochondrial membrane potential. Mech. Ageing Dev. 2009, 130:461-465.
34. Lenaerts I., van Eygen S., van Fleteren J. Adult-limited dietary restriction slows gompertzian aging in Caenorhabditis elegans. Ann. N. Y. Acad. Sci. 2007, 1100:442-448.
35. Lenaz G., Genova M.L. Supramolecular organisation of the mitochondrial respiratory chain: a new challenge for the mechanism and control of oxidative phosphorylation. Adv. Exp. Med. Biol. 2012, 748:107-144.
36. Lesnefsky E.J., Hoppel C.L. Oxidative phosphorylation and aging. Ageing Res. Rev. 2006, 5:402-433.
37. Lopez-Lluch G., Hunt N., Jones B., Zhu M., Jamieson H., Hilmer S., Cascajo M.V., Allard J., Ingram D.K., Navas P., de Cabo R. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1768-1773.
38. Maas M.F., Krause F., Dencher N.A., Sainsard-Chanet A. Respiratory complexes III and IV are not essential for the assembly/stability of complex I in fungi. J. Mol. Biol. 2009, 387:259-269.
39. Magalhaes J., Ascensao A., Soares J.M., Ferreira R., Neuparth M.J., Marques F., Duarte J.A. Acute and severe hypobaric hypoxia increases oxidative stress and impairs mitochondrial function in mouse skeletal muscle. J. Appl. Physiol. 2005, 99:1247-1253.
40. Masoro E.J. Overview of caloric restriction and ageing. Mech. Ageing Dev. 2005, 126:913-922.
41. McElwee J.J., Schuster E., Blanc E., Thomas J.H., Gems D. Shared transcriptional signature in Caenorhabditis elegans Dauer larvae and long-lived daf-2 mutants implicates detoxification system in longevity assurance. J. Biol. Chem. 2004, 279:44533-44543.
42. Miwa S., Brand M.D. Mitochondrial matrix reactive oxygen species production is very sensitive to mild uncoupling. Biochem. Soc. Trans. 2003, 31:1300-1301.
43. Morcos M., Du X., Pfisterer F., Hutter H., Sayed A.A., Thornalley P., Ahmed N., Baynes J., Thorpe S., Kukudov G., Schlotterer A., Bozorgmehr F., El Baki R.A., Stern D., Moehrlen F., Ibrahim Y., Oikonomou D., Hamann A., Becker C., Zeier M., Schwenger V., Miftari N., Humpert P., Hammes H.P., Buechler M., Bierhaus A., Brownlee M., Nawroth P.P. Glyoxalase-1 prevents mitochondrial protein modification and enhances lifespan in Caenorhabditis elegans. Aging Cell 2008, 7:260-269.
44. Mouchiroud L., Molin L., Kasturi P., Triba M.N., Dumas M.E., Wilson M.C., Halestrap A.P., Roussel D., Masse I., Dalliere N., Segalat L., Billaud M., Solari F. Pyruvate imbalance mediates metabolic reprogramming and mimics lifespan extension by dietary restriction in Caenorhabditis elegans. Aging Cell 2011, 10:39-54.
45. Neff D., Dencher N.A. Purification of multisubunit membrane protein complexes: isolation of chloroplast FoF1-ATP synthase, CFo and CF1 by blue native electrophoresis. Biochem. Biophys. Res. Commun. 1999, 259:569-575.
46. Nisoli E., Tonello C., Cardile A., Cozzi V., Bracale R., Tedesco L., Falcone S., Valerio A., Cantoni O., Clementi E., Moncada S., Carruba M.O. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 2005, 310:314-317.
47. Petrosillo G., De Benedictis V., Ruggiero F.M., Paradies G. Decline in cytochrome c oxidase activity in rat-brain mitochondria with aging. Role of peroxidized cardiolipin and beneficial effect of melatonin. J. Bioenerg. Biomembr. 2013, 45:431-440.
48. Reifschneider N.H., Goto S., Nakamoto H., Takahashi R., Sugawa M., Dencher N.A., Krause F. Defining the mitochondrial proteomes from five rat organs in a physiologically significant context using 2D blue-native/SDS-PAGE. J. Proteome Res. 2006, 5:1117-1132.
49. Ren J.C., Rebrin I., Klichko V., Orr W.C., Sohal R.S. Cytochrome c oxidase loses catalytic activity and structural integrity during the aging process in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 2010, 401:64-68.
50. Renner-Sattler K., Fasching M., Gnaiger E. Determination of membrane potential with TPP+ and an ion selective electrode system. Mitochondrial Physiol. Netw. 2010, 14(05):1-15.
51. Schäfer E., Seelert H., Reifschneider N.H., Krause F., Dencher N.A., Vonck J. Architecture of active mammalian respiratory chain supercomplexes. J. Biol. Chem. 2006, 281:15370-15375.
52. Schäfer E., Dencher N.A., Vonck J., Parcej D.N. Three-dimensional structure of the respiratory chain supercomplex I1III2IV1 from bovine heart mitochondria. Biochemistry 2007, 46:12579-12585.
53. Schagger H. Respiratory chain supercomplexes of mitochondria and bacteria. Biochim. Biophys. Acta 2002, 1555:154-159.
54. Schulz T.J., Zarse K., Voigt A., Urban N., Birringer M., Ristow M. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 2007, 6:280-293.
55. Seelert H., Dani D.N., Dante S., Hauss T., Krause F., Schäfer E., Frenzel M., Poetsch A., Rexroth S., Schwassmann H.J., Suhai T., Vonck J., Dencher N.A. From protons to OXPHOS supercomplexes and Alzheimer's disease: structure-dynamics-function relationships of energy-transducing membranes. Biochim. Biophys. Acta 2009, 1787:657-671.
56. Sohal R.S., Ku H.H., Agarwal S., Forster M.J., Lal H. Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse. Mech. Ageing Dev. 1994, 74:121-133.
57. Suthammarak W., Yang Y.Y., Morgan P.G., Sedensky M.M. Complex I function is defective in complex IV-deficient Caenorhabditis elegans. J. Biol. Chem. 2009, 284:6425-6435.
58. Suthammarak W., Morgan P.G., Sedensky M.M. Mutations in mitochondrial complex III uniquely affect complex I in Caenorhabditis elegans. J. Biol. Chem. 2010, 285:40724-40731.
59. Szewczyk N.J., Udranszky I.A., Kozak E., Sunga J., Kim S.K., Jacobson L.A., Conley C.A. Delayed development and lifespan extension as features of metabolic lifestyle alteration in C. elegans under dietary restriction. J. Exp. Biol. 2006, 209:4129-4139.
60. TeKippe M., Aballay A. C. elegans germline-deficient mutants respond to pathogen infection using shared and distinct mechanisms. PLoS One 2010, 5:e11777.
61. van Diepeningen A.D., Maas M.F., Huberts D.H., Goedbloed D.J., Engelmoer D.J., Slakhorst S.M., Koopmanschap A.B., Krause F., Dencher N.A., Sellem C.H., Sainsard-Chanet A., Hoekstra R.F., Debets A.J. Calorie restriction causes healthy life span extension in the filamentous fungus Podospora anserina. Mech. Ageing Dev. 2010, 131:60-68.
62. Vanfleteren J.R. Large scale cultivation of a free-living nematode (Caenorhabditis elegans). Separatum Experientia 1976, 32:1087-1088.
63. Vanfleteren J.R., Braeckman B.P. Mechanisms of life span determination in Caenorhabditis elegans. Neurobiol. Aging 1999, 20:487-502.
64. Wernicke C., Hellmann J., Zieba B., Kuter K., Ossowska K., Frenzel M., Dencher N.A., Rommelspacher H. 9-Methyl-beta-carboline has restorative effects in an animal model of Parkinson's disease. Pharmacol. Rep. 2010, 62:35-53.
65. Wittig I., Schagger H. Supramolecular organization of ATP synthase and respiratory chain in mitochondrial membranes. Biochim. Biophys. Acta 2009, 1787:672-680.
66. Wittig I., Carrozzo R., Santorelli F.M., Schagger H. Supercomplexes and subcomplexes of mitochondrial oxidative phosphorylation. Biochim. Biophys. Acta 2006, 1757:1066-1072.
67. Yuan Y., Kadiyala C.S., Ching T.T., Hakimi P., Saha S., Xu H., Yuan C., Mullangi V., Wang L., Fivenson E., Hanson R.W., Ewing R., Hsu A.L., Miyagi M., Feng Z. Enhanced energy metabolism contributes to the extended life span of calorie-restricted Caenorhabditis elegans. J. Biol. Chem. 2012, 287:31414-31426.